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Coevolution of parasites and hosts 1) Evolution of host-parasite interactions 2) Evolution of virulence 3) Trade-offs in host defense 4) Brood parasitism - an arms race? 5) End of arms race? 6) Example exam questions
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Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

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Page 1: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Coevolution of parasites and hosts

1) Evolution of host-parasite interactions

2) Evolution of virulence

3) Trade-offs in host defense

4) Brood parasitism - an arms race?

5) End of arms race?

6) Example exam questions

Page 2: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Parasitism:Individuals of one species live on or in members of another species, which are not killed immediately.

One party (parasite) gains at the expense of the other (host).

Coevolution (strictly):

Reciprocal evolutionary change of interacting species

1) Evolution of host-parasite interactions

Page 3: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Ÿ immune systems and pathogens

Ÿ chemical and physical defenses against phytophagous insects (e.g., Heliconius caterpillars on Passiflora vines)

Ÿ brood parasitism (e.g., cuckoos and hosts)

Ÿ kleptoparasitism (e.g., frigate birds)

Ÿ interspecific “slavery” (e.g., ants)

1) Evolution of host-parasite interactions

Page 4: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Colony foundation by Epimyrma queens follows the typical pattern seen in many temporary social parasites and obligatory slave makers, and involves the forceful usurpation of a host colony. ... E. kraussei queens approach host colonies in an aggressive manner. Once the parasite penetrates the host nest, she kills the host queen and is adopted by the host workers.

The queens of E. ravouxi use a more 'conciliatory' approach initially, grooming and stroking host workers, but, once inside the nest, the parasite mounts the host queen from behind and kills her by seizing her around the neck with her sabre-shaped mandibles.

Interspecific slavery in ants

Photo of E. ravouxi by Olivier Delattrehttp://the-scorpion-and-the-frog.blogspot.ca/2012_10_01_archive.html

E. stumperi queens crouch down, freeze and seem to feign death during their initial encounters with host workers, but subsequently begin to mount workers from behind and to groom them, perhaps acquiring chemical recognition cues in the process. However, once inside the nest, the parasite queen systematically eliminates the host queens by mounting them, rolling them over and grasping their necks in her mandibles until they succumb.

- Lewis, et al, eds. 2002. The behavioural ecology of parasites. CABI.

1) Evolution of host-parasite interactions

Page 5: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

The conventional wisdom once was that parasites should evolve reduced virulence to their hosts.

This was based on observations that

- some mutualistic associations have evolved from once-pathogenic interactions (lichens? mycorrhizal fungi?).

- highly virulent parasites kill their hosts, and thereby themselves.

- examples of attenuation of virulence in some disease outbreaks

2) Evolution of virulence

Page 6: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

An alternative perspective is that selection should favor genotypes whose level of virulence maximizes their rate of increase.

Those are not necessarily the genotypes with the lowest virulence.

The optimum virulence is likely to depend on a balance between the advantages of high virulence (rapid multiplication leading to increased transmission rate) and disadvantages of high virulence (increased host mortality).

Consequently, with selection might often favor an intermediate degree of virulence.

2) Evolution of virulence

Page 7: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Evolution of Myxoma virulence

2) Evolution of virulence

Page 8: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

100

150

200

250

Rabbit a

bundance

Rabbit fleas introducedMyxomatosis introduced

Recorded rabbit plagues

0

50

1927

1931

1935

1939

1943

1947

1951

1955

1959

1963

1967

1971

1975

1979

1983

1987

1991

1995

1999

2003

2007

Rabbit abundance in northeast South Australia accompanyingrapid evolution of lower virulence by viruses (and of resistance by rabbits)

Saunders et al (2010) Biol Control

Rabbit HemorrhagicDisease introduced

2) Evolution of virulence

Page 9: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Evolution of Myxoma virulence

2) Evolution of virulence

Page 10: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Parasite: barley stripe mosaic virus

Host: barley (Hordeum vulgare)

vertical transmissiontreatment

(4 barley generations,transmission by seeds)

horizontal transmission treatment (4 barley generations)

Stewart et at. (2005)

http://www.albertabarley.com/barley/barley/images/BarleyCommission-stock4.JPG

Experimental evolution of virulence2) Evolution of virulence

Page 11: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

“virulence” measured bynumber of viable seeds produced by infected plant

Stewart et at. (2005)1 – (viable seeds of infected plants) / (viable seeds of control plants) x 100%

horizontal transmission treatment (4 barley generations)

2) Evolution of virulence

Page 12: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Stewart et at. (2005)

vertical transmission treatment

2) Evolution of virulence

Page 13: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Re

lati

ve

fre

qu

en

cy

Virulence (% deaths per infection)

Re

lati

ve

fre

qu

en

cy

0.01 0.1

0.6

0.8

0.4

0.4

0.6

0.2

0.2

0.0

0.0

Ewald (1993)

1.0 10.0 100.0

Diseases transmitted directly

Diseases transmitted byinsect vector

Virulence and mode of transmission of human diseases

2) Evolution of virulence

Page 14: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Ewald (1993)

Waterborne human diseases are deadly

Outb

reaks

of dis

ease

cause

d b

yw

ate

rborn

e p

ath

ogens

(% o

f to

tal)

Virulence (% of deaths per infection)

2) Evolution of virulence

Page 15: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Coevolution between wild parsnip and the parsnip webworm

Negative genetic correlations between leaf secondary compounds (furanocoumarins) and indices of flower size

Berenbaum et al (1986)

Cost of defense in wild parsnip

http://www.ontariowildflower.com/lakeedge.htm

3) Trade-offs in host defense

Page 16: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Zangerl & Berenbaum 2005

Wild parsnip was introduced to North America before the parsnip webworm. In the 1800's, concentrations of furanocoumarins in parsnip seeds in herbarium specimens were lower than that in Old World plants (indicated by horizontal bars). Furanocoumarin concentrations rose after webworm damage began to appear (1900's).

http://mothphotographersgroup.msstate.edu/larva.php?plate=01.0&sort=h© N. Schneider

Coevolution between wild parsnip and the parsnip webworm

3) Trade-offs in host defense

Page 17: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Coevolution between European cuckoos and hosts

reed warbler

reed warbler nest

cuckoo chick

http://fleetpond.wordpress.com/2009/05/

4) Brood parasitism - an arms race?

Page 18: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Adaptation: Nest parasitism by European cuckoos

Newly-hatched cuckoo chickejecting host eggs and chicks

4) Brood parasitism - an arms race?

Hosts frequently parasitized by common cuckoo in the UK are reed warbler, meadow pipit, pied wagtail, and dunnock.

Page 19: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Pied wagtail

Dunnock

Reed warb

ler

Meadow pipit

reject

keep

Frequency of rejection by reed warblers of rubber model cuckoo eggs placed in their nests

Type of model cuckoo egg added to nest

Num

be

r of nest

s

0

5

10

15

20

Counteradaptation: Host species have evolved rejection of eggs unlike their own

Brooke & Davies (1988)

4) Brood parasitism - an arms race?

Page 20: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

28 5

30 22

27 5

11 23

Britaincuckoospresent

Icelandcuckoosabsent

Reject

Keep

Reject

Keep

Meadow pipit

Pied/white wagtail

Davies & Brooke (1989)

4) Brood parasitism - an arms race?Counteradaptation:

Host species have evolved rejection of eggs unlike their own

Host populations in Iceland, where cuckoos are absent, are less likely to reject eggs unlike their own than in Britain, where cuckoos are present.

Page 21: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

robin

pied wagtail

dunnock

reed warbler

meadow pipit

host cuckoo model

Counter-counter adaptation:Cuckoos have evolved egg mimicry (or not, in case of dunnock)

4) Brood parasitism - an arms race?

Brooke & Davies (1988)

Page 22: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Meadow pipit

Dunnock

Reedwarbler

http://www.britannica.com/EBchecked/topic-art/128222/21/Coevolution-of-one-species-with-many-species

4) Brood parasitism - an arms race?Counter-counter adaptation:

Cuckoos have evolved egg mimicry (or not, in case of dunnock)

Page 23: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

4) Brood parasitism - an arms race?Counter-counter adaptation:

Cuckoos have evolved egg mimicry (or not, in case of dunnock)

Stoddard & Stevens (2011) Evolution

´

Host rejection rate of nonmimetic eggs and mean “just noticeable differences” (JND - a composite metric) between cuckoo and host eggs in background color and background luminance. Data from continental Europe. Closer mimicry is associated with higher rejection rates of eggs unlike the hosts’ own.

Page 24: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Counter-counter adaptation:Cuckoos have evolved hawk-like ‘chuckle’ call

4) Brood parasitism - an arms race?

Pro

ba

bili

ty o

f e

gg

acc

ep

tan

ce

0.0

0.2

0.4

0.6

0.8

1.0

6/18 6/17 13/17 13/18

a b

Collareddove

Malecuckoo

Femalecuckoo

Sparrowhawk

Fig. 2 | Reed warblers were more likely to accept a foreign egg after playback of female cuckoo or hawk calls than after the calls of a male cuckoo or

dove. a, A reed warbler clutch with one egg painted brown to simulate parasitism. b, The probability of reed warblers accepting a foreign egg one day after

the experiment was greater after exposure to female cuckoo or hawk calls compared with dove or male cuckoo calls (experiment 3 in Table ; n =1  70 nests;

data are predicted means ±  s.e.m.; the raw proportions of the nests in which foreign eggs were accepted are also shown at the base of each bar). Male 2cuckoo calls had no more effect than control dove calls  =(χ  0.015; P =  0.90), whereas female cuckoo calls reduced egg rejection as much as hawk calls

2(χ  =  0.083; P =  0.77).

York & Davies (2017) Nature Ecology & Evolution

Page 25: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

4) Brood parasitism - an arms race?Counter-counter adaptation:

Cuckoos have evolved egg mimicry (or not, in case of dunnock)

The paradox of the dunnock - why no egg rejection?

https://www.rspb.org.uk/birds-and-wildlife/bird-and-wildlife-guides/bird-a-z/d/dunnock/

Page 26: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Absence of chick recognition by hosts

Rate of food provisioning to cuckoo chickscompared to other chicks

Davies et al. (1998)

Loads

bro

ught per

hour

Chick species

4) Brood parasitism - an arms race?

Page 27: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Davies et al. (1998)

Single reed warbler chick

Brood of 4 reed warbler chicks

One cuckoo chick

One blackbird chick

Loads

bro

ught per

hour

Begging sound played

4) Brood parasitism - an arms race?

Provisioning rate by reed warbler parents (mean + 1SE) to single blackbird (n=6) or song thrush (n=3) chicks tested with no sound, sound of cuckoo chick begging, or sound of a brood of four reed warblers.

Cuckoo chicks have evolved begging call like that of host (reed warbler)

Sonograms of begging calls (recorded 60 min after feeding to satiation)

Page 28: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Davies & Brooke (1989)

Some non-host species have evolved high egg rejection rates

5) End of arms race?

Percent of nests rejecting unlike model eggs

Perc

en

t of sp

eci

es

0

20

40

60

80

0 20 40 60 80 100

unsuitable hosts

suitable rare hosts

0

20

40

60

80

current hosts

Page 29: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Davies & Brooke (1989)

Some non-host species have evolved high egg rejection rates

Percent of nests rejecting unlike model eggs

Perc

en

t of sp

eci

es

0

20

40

60

80

0 20 40 60 80 100

unsuitable hosts

suitable rare hosts

0

20

40

60

80

current hosts

linnetgreenfinchbullfinch

chaffinch

Feed seeds to young

Feeds insects to young

5) End of arms race?

Page 30: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

Davies & Brooke (1989)

Some non-host species have evolved high egg rejection rates

Percent of nests rejecting unlike model eggs

Perc

en

t of sp

eci

es

0

20

40

60

80

0 20 40 60 80 100

unsuitable hosts

suitable rare hosts

0

20

40

60

80

current hosts

pied flycatcher

spotted flycatcher

Nests in treeholes

Has open nest

5) End of arms race?

Page 31: Coevolution of parasites and hosts - | Department of Zoology at …bio418/08 host-parasite... · 2019-10-15 · cuckoo calls had no more effect than control dove calls =(2 χ 0.015;

6) Example exam questions

Why are some parasites more virulent than others? Present a study design for testing alternative hypotheses.

Consider a coevolutionary interaction between a disease and its host. Under what circumstances might we expect natural selection to favor a low virulence of the disease? Under what circumstances might we expect natural selection to favor a high virulence of the disease? Explain.

Is the coevolution between cuckoo brood parasites and their avian hosts best described as an arms race or as steady-state coevolution (in the language of Abrams)? Explain your reasoning.

Is the coevolution between wild parsnip and the parsnip webworm best described as an arms race or as steady-state coevolution (in the language of Abrams)? Explain your reasoning.

Suggest a hypothesis for why waterborne human pathogens are often highly virulent. Explain the basis for your hypothesis, and suggest an experimental test.